MOLECULAR PLANT PATHOLOGY 2013 PATHOGEN PROFILE

Pathogen profile

Fusarium culmorum: causal agent of foot and root rot and headblight on wheat

BARBARA SCHERM1, VIRGIL IO BALMAS1, FRANCESCA SPANU1, GIOVANNA PANI1,2,GIOVANNA DELOGU2, MATIAS PASQUALI3 AND QUIRICO MIGHELI 1,*1Dipartimento di Agraria—Sezione di Patologia Vegetale ed Entomologia and Centro Interdisciplinare per lo Sviluppo della Ricerca Biotecnologica e per lo Studio dellaBiodiversità della Sardegna e dell'Area Mediterranea, Università degli Studi di Sassari, Via E. De Nicola 9, I-07100 Sassari, Italy2Istituto CNR di Chimica Biomolecolare, Traversa La Crucca, 3, I-07100 Sassari, Italy3Centre de Recherche—Gabriel Lippmann, 41, rue du Brill, L-4422 Belvaux, Luxembourg

SUMMARY

Fusarium culmorum is a ubiquitous soil-borne fungus able tocause foot and root rot and Fusarium head blight on differentsmall-grain cereals, in particular wheat and barley. It causes sig-nificant yield and quality losses and results in contamination ofthe grain with mycotoxins.This review summarizes recent researchactivities related to F. culmorum, including studies into its popu-lation diversity, mycotoxin biosynthesis, mechanisms of pathogen-esis and resistance, the development of diagnostic tools andpreliminary genome sequence surveys. We also propose potentialresearch areas that may expand our basic understanding of thewheat–F. culmorum interaction and assist in the management ofthe disease caused by this pathogen.Taxonomy: Fusarium culmorum (W.G. Smith) Sacc. KingdomFungi; Phylum Ascomycota; Subphylum Pezizomycotina; Class Sor-dariomycetes; Subclass Hypocreomycetidae; Order Hypocreales;Family Nectriaceae; Genus Fusarium.Disease symptoms: Foot and root rot (also known as Fusariumcrown rot): seedling blight with death of the plant before or afteremergence; brown discoloration on roots and coleoptiles of theinfected seedlings; brown discoloration on subcrown internodesand on the first two/three internodes of the main stem; tillerabortion; formation of whiteheads with shrivelled white grains;Fusarium head blight: prematurely bleached spikelets or blightingof the entire head, which remains empty or contains shrunkendark kernels.Identification and detection: Morphological identification isbased on the shape of the macroconidia formed on sporodochiaon carnation leaf agar. The conidiophores are branched monophi-alides, short and wide. The macroconidia are relatively short andstout with an apical cell blunt or slightly papillate; the basal cell isfoot-shaped or just notched. Macroconidia are thick-walled andcurved, usually 3–5 septate, and mostly measuring 30–50 ¥ 5.0–7.5 mm. Microconidia are absent. Oval to globose chlamydosporesare formed, intercalary in the hyphae, solitary, in chains or in

clumps; they are also formed from macroconidia.The colony growsvery rapidly (1.6–2.2 cm/day) on potato dextrose agar (PDA) at theoptimum temperature of 25 °C. The mycelium on PDA is floccose,whitish, light yellow or red. The pigment on the reverse plate onPDA varies from greyish-rose, carmine red or burgundy. A widearray of polymerase chain reaction (PCR) and real-time PCR tools,as well as complementary methods, which are summarised in thefirst two tables, have been developed for the detection and/orquantification of F. culmorum in culture and in naturally infectedplant tissue.Host range: Fusarium culmorum has a wide range of hostplants, mainly cereals, such as wheat, barley, oats, rye, corn,sorghum and various grasses. In addition, it has been isolated fromsugar beet, flax, carnation, bean, pea, asparagus, red clover, hop,leeks, Norway spruce, strawberry and potato tuber. Fusarium cul-morum has also been associated with dermatitis on marram grassplanters in the Netherlands, although its role as a causal agent ofskin lesions appears questionable. It is also isolated as a symbiontable to confer resistance to abiotic stress, and has been proposedas a potential biocontrol agent to control the aquatic weedHydrilla spp.Useful websites: http://isolate.fusariumdb.org/; http://sppadbase.ipp.cnr.it/; http://www.broad.mit.edu/annotation/genome/fusarium_group/MultiHome.html; http://www.fgsc.net/Fusarium/fushome.htm; http://plantpath.psu.edu/facilities/fusarium-research-center; http://www.phi-base.org/; http://www.uniprot.org/; http://www.cabi.org/; http://www.indexfungorum.org/

INTRODUCTION

Fusarium culmorum (W.G. Smith) Sacc. is a ubiquitous soil-bornefungus with a highly competitive saprophytic capability. As a fac-ultative parasite, it is able to cause foot and root rot (FRR) andFusarium head blight (FHB) on different small-grain cereals, inparticular wheat and barley. Fusarium culmorum is also known as*Correspondence: Email: [email protected]

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MOLECULAR PLANT PATHOLOGY (2013) 14 (4) , 323–341 DOI: 10.1111/mpp.12011

© 2012 BSPP AND BLACKWELL PUBLISHING LTD 323

a post-harvest pathogen, especially on freshly harvested grain thathas not been dried or stored properly (Aldred and Magan, 2004;Eifler et al., 2011; Lowe et al., 2012; Magan et al., 2003, 2010).Together with F. graminearum Schwabe (teleomorph Gibberellazeae) and F. pseudograminearum O’Donnell and Aoki (teleomorphGibberella coronicola), F. culmorum has been reported as one ofthe main pathogens of wheat worldwide (Burgess et al., 2001;Goswami and Kistler, 2004; Hogg et al., 2010; Kosiak et al., 2003;Miedaner et al., 2008; Treikale et al., 2010; Wagacha andMuthomi, 2007; Wang et al., 2006).

Yield and quality losses are particularly important when F. cul-morum induces FHB, which develops from infection at anthesisand spreads until grain harvest, causing grain contamination withmycotoxins, such as type B trichothecenes, zearalenone andfusarins (Hope et al., 2005; Jennings et al., 2004; Kammoun et al.,2010; Lacey et al., 1999; Placinta et al., 1999; Rohweder et al.,2011; Visconti and Pascale, 2010). The sesquiterpene epoxide tri-chothecenes are considered to be the most bioactive compoundsproduced by F. culmorum. These mycotoxins are able to inhibiteukaryotic protein synthesis (Wei and McLaughlin, 1974) andcause toxicoses in humans or animals consuming contaminatedfood or feed (Sudakin, 2003). They have also been reported toinduce apoptosis (Desmond et al., 2008; Yang et al., 2000) andplay an important role as virulence factors (Bai et al., 2002; Desjar-dins et al., 1996, 2000; Harris et al., 1999; Jansen et al., 2005;Maier et al., 2006; McCormick, 2003; Proctor et al., 1995, 2002;Scherm et al., 2011; Ward et al., 2008; Zhang et al., 2010).

The purpose of this profile is to provide an overview of therecent research activities related to F. culmorum, including thoseon population diversity, mycotoxin biosynthesis, mechanisms ofpathogenesis and resistance, the development of diagnostic toolsand preliminary genome sequence surveys (see Tables 1 and 2,respectively, for a list of PCR-based and non PCR-basedapproaches to discriminate and detect F. culmorum). We alsopropose potential research areas that may expand our basicunderstanding of the wheat–F. culmorum interaction and ulti-mately assist in the management of the different facies of thedisease caused by this pathogen.

DISEASE SYMPTOMS

Fusarium culmorum causes two distinct diseases on wheat: FRRand FHB, also known as ear blight or scab. FRR symptoms varydepending on the time of infection: if the fungus attacks at theearly stage, just after sowing, pre- and post-emergence seedlingdeath occurs, with brown discoloration on the coleoptiles, rootsand the pseudostem; if the infection starts later in the season,brown lesions appear on the first two or three internodes of themain stem and tiller abortion occurs (Fig. 1B). In the presence ofhigh humidity, a reddish-pink discoloration is often evident on thenodes caused by the presence of sporulating mycelium (Fig. 1C).

The presence of whiteheads with shrivelled grain—or no grain atall—is easily observed when the wheat is still immature(Fig. 1D,E). Infected plants are more prone to lodging. FHB symp-toms include partial head blighting, with the appearance of one ormore prematurely bleached spikelets, or blighting of the entirehead, which is easily observed when wheat has not yet reachedthe ripening stage (Fig. 2A,B). Initially, infected spikelets showlight-brown, water-soaked spots on the glumes, which thenbecome dark brown. Infected spikelets remain empty or containshrunken grey/brown kernels. Browning on the rachilla and therachis can be observed and, under favourable conditions, thefungus may infect the stem below the head, inducing a brown/purplish discoloration (Fig. 2C). Pink to orange sporodochia maybe evident at the base of the spikelets or between the glumes andlemmas, if the environmental conditions are particularly humid(Fig. 2D,F).

EPIDEMIOLOGY

Fusarium culmorum has been traditionally reported as the incitantof FHB in northern, central and western Europe (Muthomi et al.,2000;de Nijs et al., 1997; Parry et al., 1995). However, recently, innorthern Europe, a change is being observed in the frequency ofisolation, and F. culmorum is seldom reported compared withF. graminearum. This progressive switch may be explained by thewidespread use of feed maize as a rotation crop with wheat innorthern Europe, with consequent F. graminearum inoculumbuild-up in the soil. It is noteworthy that F. culmorum is occasion-ally isolated from maize crops and maize kernels, but never as themain pathogen (Logrieco et al., 2002; Scauflaire et al., 2011; VanAsselt et al., 2012). Other reasons for the transition from F. cul-morum to F. graminearum may be related to the gradual adapta-tion of F. graminearum to colder climates as a result of genomeplasticity (Lysøe et al., 2011; Raffaele and Kamoun, 2012) or to therise in average temperatures caused by climate change (Jenningset al., 2004; Waalwijk et al., 2003; West et al., 2012; Xu et al.,2005). However, in Luxembourg, following the year 2011 withhardly any precipitation in May, 90% of the blighted spikes wereinfected by F. culmorum, whereas only 10% were infected byF. graminearum, suggesting a role of climatic conditions in drivingthe prevalence of each species, reversing drastically the previousspecies distribution (Giraud et al., 2010).

Contrary to early reports from colder areas in central and north-ern Europe, F. culmorum is now frequently reported as the mainagent of FHB in the Mediterranean region, and particularly in yearscharacterized by wet conditions during the phenological phases offlowering and kernel filling (Corazza et al., 2002; Fakhfakh et al.,2011; Kammoun et al., 2010; Pancaldi et al., 2010). The greaterincidence of FHB caused by F. culmorum in these areas is correlatedwith its presence as the main cause of FRR, a disease that is par-ticularly severe on durum wheat in southern Italy and North Africa.

324 B. SCHERM et al .

MOLECULAR PLANT PATHOLOGY (2013) 14(4 ) , 323–341 © 2012 BSPP AND BLACKWELL PUBLISHING LTD

Tabl

e1

Sum

mar

yof

publ

ished

prim

ers

used

fors

pecie

san

dch

emot

ype

dete

rmin

atio

nin

Fusa

rium

culm

orum

.

Iden

tifica

tion

ofPr

imer

san

dpr

obes

(5′→

3′)

Targ

etDN

APC

Rte

chni

que

Refe

renc

e

Spec

ies

(F.c

ulm

orum

and

F.gr

amin

earu

m)

FcF

CAAA

AGCT

TCCC

GAG

TGTG

TCFc

RG

GCG

AAG

GTT

CAAG

GAT

GAC

Unkn

own

Conv

entio

nalP

CRBa

turo

-Cie

snie

wsk

aan

dSu

chor

zyns

ka(2

011)

;Doo

han

etal

.(19

98)

Spec

ies

(not

able

todi

stin

guish

from

F.ce

real

is)Fc

ulC5

61fw

dCA

CCG

TCAT

TGG

TATG

TTG

TCAC

TFc

ulC6

14re

vCG

GG

AGCG

TCTG

ATAG

TCG

ef1-

aRe

al-ti

me

PCR

Nico

laise

net

al.(

2009

)

Spec

ies

(toge

ther

with

Fce

real

isan

dF.

gram

inea

rum

)FI

P-hy

d5G

CACA

GCA

CTG

GG

AAG

TGCG

AGAA

GCG

ACAG

GCC

TACA

BIP-

hyd5

TGG

GTG

TTG

CTG

ACCT

CGAC

GG

GG

CTG

TTCA

TGTT

AGCT

B3-h

yd4

GAC

AGCG

CTG

AAG

TTG

TCLo

opB-

hyd5

CCG

TAAG

TACT

CGAG

TCTG

Loop

F-hy

d5G

TAG

AGG

CCAC

TGCA

AGG

F3-h

yd5

CTTG

GAG

CCG

TTG

TCTC

TG

Hyd

5LA

MP

PCR

Dens

chla

get

al.(

2012

)

Spec

ies

(toge

ther

with

F.cr

ockw

elle

nse)

CRO

-Cfw

dCT

CAG

TGTC

CACC

GCG

TTG

CGTA

GTG

TCR

O-C

rev

AAG

CAG

GAA

ACAG

AAAC

CCTT

TCC

RAPD

fragm

ent

Conv

entio

nalP

CRYo

dera

ndCh

ristia

nson

(199

8)

Spec

ies

(toge

ther

with

F.gr

amin

earu

m)

CUL-

Afw

dTT

TCAG

CGG

GCA

ACTT

TGG

GTA

GA

CUL-

Are

vAA

GCT

GAA

ATAC

GCG

GTT

GAT

AGG

RAPD

fragm

ent

Conv

entio

nalP

CRYo

dera

ndCh

ristia

nson

(199

8)

Spec

ies

C51E

ND

fwd

AACT

GAA

TTG

ATCG

CAAG

CC5

1EN

Dre

vCC

CTTC

TTAC

GCC

AATC

TCUn

know

nRe

al-ti

me

PCR

Cova

relli

etal

.(20

12)

Spec

ies

OPT

18F4

70G

ATG

CCAG

ACCA

AGAC

GAA

GO

PT18

R470

GAT

GCC

AGAC

GCA

CTAA

GAT

SCAR

Conv

entio

nalP

CRRe

al-ti

me

PCR*

Batu

ro-C

iesn

iew

ska

and

Such

orzy

nska

(201

1);B

rand

fass

and

Karlo

vsky

2006

;Sc

hilli

nget

al.(

1996

)Sp

ecie

sFc

92s1

forw

ard

TTCA

CTAG

ATCG

TCCG

GCA

GFc

92s1

reve

rse

GAG

CCCT

CCAA

GCG

AGAA

GUn

know

nRe

al-ti

me

PCR

Leiso

vaet

al.(

2006

)

Spec

ies

Fc01

FAT

GG

TGAA

CTCG

TCG

TGG

CFc

01R

CCCT

TCTT

ACG

CCAA

TCTC

GRA

PDfra

gmen

tCo

nven

tiona

lPCR

Batu

ro-C

iesn

iew

ska

and

Such

orzy

nska

(201

1);N

ichol

son

etal

.(19

98)

Spec

ies

Fcg1

7FTC

GAT

ATAC

CGTG

CGAT

TTCC

Fcg1

7RTA

CAG

ACAC

CGTC

AGG

GG

GRA

PDfra

gmen

tCo

nven

tiona

lPCR

Batu

ro-C

iesn

iew

ska

and

Such

orzy

nska

(201

1);N

ichol

son

etal

.(19

98)

Spec

ies

175F

TTTT

AGTG

GAA

CTTC

TGAG

TAT

430R

AGTG

CAG

CAG

GAC

TGCA

GC

ITS

regi

onFl

uore

scen

t-lab

elle

dPC

R-ba

sed

assa

yM

ishra

etal

.(20

03)

Spec

ies

culm

orum

MG

B-R

GAA

CGCT

GCC

CTCA

AGCT

Tcu

lmor

umM

GB-

FTC

ACCC

AAG

ACG

GG

AATG

APr

obe

CACT

TGG

ATAT

ATTT

CC

Gen

omic

DNA

Real

-tim

ePC

R(T

aqM

an)

Waa

lwijk

etal

.(20

04)

Type

Btri

chot

hece

nepr

oduc

ers

Fcu-

FG

ACTA

TCAT

TATG

CTTG

CGAG

AGFg

c-R

CTCT

CATA

TACC

CTCC

GIG

Sre

gion

Conv

entio

nalP

CRBa

turo

-Cie

snie

wsk

aan

dSu

chor

zyns

ka(2

011)

;Jur

ado

etal

.(20

05)

15-A

DON

subc

hem

otyp

eTr

i3F9

71CA

TCAT

ACTC

GCT

CTG

CTG

Tri3

R167

9TT

(AG

)TAG

TTTG

CATC

ATT(

AG)T

AGTR

I3Co

nven

tiona

lPCR

Pasq

uali

etal

.(20

11);

Qua

rtaet

al.

(200

6)3-

ADO

Nsu

bche

mot

ype

Tri3

F132

5G

CATT

GG

CTAA

CACA

TGA

Tri3

R167

9TT

(AG

)TAG

TTTG

CATC

ATT(

AG)T

AGTR

I3Co

nven

tiona

lPCR

Pasq

uali

etal

.(20

11);

Qua

rtaet

al.

(200

6)N

ivale

nols

ubch

emot

ype

Tri7

F340

ATCG

TGTA

CAAG

GTT

TACG

Tri7

R965

TTCA

AGTA

ACG

TTCG

ACAA

TTR

I7Co

nven

tiona

lPCR

Pasq

uali

etal

.(20

11);

Qua

rtaet

al.

(200

5)Hi

gh-d

eoxy

niva

leno

l-pro

ducin

gst

rain

sN

1-2

CTTG

TTAA

GCT

AAG

CGTT

TTN

1-2R

AACC

CCTT

TCCT

ATG

TGTT

ATR

I6/T

RI5

inte

rgen

icre

gion

Conv

entio

nalP

CRBa

kan

etal

.(20

02)

Low

-deo

xyni

vale

nol-p

rodu

cing

stra

ins

4056

ATCC

CTCA

AAAA

CTG

CCG

CT35

51AC

TTTC

CCAC

CGAG

TATT

TCTR

I6/T

RI5

inte

rgen

icre

gion

Conv

entio

nalP

CRBa

kan

etal

.(20

02)

The wheat pathogen Fusarium culmorum 325

© 2012 BSPP AND BLACKWELL PUBLISHING LTD MOLECULAR PLANT PATHOLOGY (2013) 14(4 ) , 323–341

Tabl

e1

Cont

inue

d.

Iden

tifica

tion

ofPr

imer

san

dpr

obes

(5′→

3′)

Targ

etDN

APC

Rte

chni

que

Refe

renc

e

Spec

ies

(toge

ther

with

F.gr

amin

earu

man

dF.

pseu

dogr

amin

earu

m)

Gze

ae87

Tfo

rwar

dCG

CATC

GAG

AATT

TGCA

Gze

ae87

Tre

vers

eTG

GCG

AGG

CTG

AGCA

AAG

Gze

ae87

Tpr

obe

6FAM

-TG

CTTA

CAAC

AAG

GCT

GCC

CACC

A-TA

MRA

TRI5

Real

-tim

ePC

R(T

aqM

an)

Stra

usba

ugh

etal

.(20

05)

Deox

yniva

leno

l-pro

ducin

giso

late

s(F

.gra

min

earu

man

dF.

culm

orum

)22

FAA

TATG

GAA

AACG

GAG

TTCA

TCTA

CA12

2RAT

TGCC

GG

TGCC

TGAA

AGT

TRI6

-TRI

5in

terg

enic

regi

onRe

al-ti

me

PCR

(SYB

RG

reen

I)Te

rzie

tal.

(200

7)

PKS1

3-co

ntai

ning

stra

ins

(F.c

ulm

orum

and

F.gr

amin

earu

m)

ZEA

-FCT

GAG

AAAT

ATCG

CTAC

ACTA

CCG

ACZE

A-R

CCCA

CTCA

GG

TTG

ATTT

TCG

TCPK

S13

Conv

entio

nalP

CR/R

eal-t

ime

PCR

(SYB

RG

reen

I)At

ouie

tal.

(201

2)

Deox

yniva

leno

l-pro

ducin

gst

rain

Tri7

FTG

CGTG

GCA

ATAT

CTTC

TTCT

ATr

i7D

ON

GTG

CTAA

TATT

GTG

CTAA

TATT

GTG

CTR

I7Co

nven

tiona

lPCR

Batu

ro-C

iesn

iew

ska

and

Such

orzy

nska

(201

1);C

hand

lere

tal.

(200

3)De

oxyn

ivale

nol-p

rodu

cing

stra

inTr

i13F

CATC

ATG

AGAC

TTG

TKCR

AGTT

TGG

GC

Tri1

3DO

NR

GCT

AGAT

CGAT

TGTT

GCA

TTG

AGTR

I13

Conv

entio

nalP

CRBa

turo

-Cie

snie

wsk

aan

dSu

chor

zyns

ka(2

011)

;Cha

ndle

reta

l.(2

003)

Niva

leno

l-pro

ducin

gst

rain

Tri7

FTG

CGTG

GCA

ATAT

CTTC

TTCT

ATr

i7N

IVTG

TGG

AAG

CCG

CAG

ATR

I7Co

nven

tiona

lPCR

Batu

ro-C

iesn

iew

ska

and

Such

orzy

nska

(201

1);C

hand

lere

tal.

(200

3)N

ivale

nol-p

rodu

cing

stra

inTr

i13N

IVF

CCAA

ATCC

GAA

AACC

GCA

Tri1

3RTT

GAA

AGCT

CCAA

TGTC

GTG

TRI1

3Co

nven

tiona

lPCR

Batu

ro-C

iesn

iew

ska

and

Such

orzy

nska

(201

1);C

hand

lere

tal.

(200

3)3-

ADO

N-p

rodu

cing

stra

inTr

i303

FG

ATG

GCC

GCA

AGTG

GA

Tri3

03R

GCC

GG

ACTG

CCCT

ATTG

TRI3

Conv

entio

nalP

CRBa

turo

-Cie

snie

wsk

aan

dSu

chor

zyns

ka(2

011)

;Jen

ning

set

al.(

2004

)Tr

ichot

hece

nepr

oduc

erTo

x5-1

GCT

GCT

CATC

ACTT

TGCT

CAG

Tox5

-2CT

GAT

CTG

GTC

ACG

CTCA

TCTR

I5Co

nven

tiona

lPCR

Batu

ro-C

iesn

iew

ska

and

Such

orzy

nska

(201

1);N

iess

enan

dVo

gel(

1998

)N

ivale

nol-p

rodu

cing

stra

in12

NF

TCTC

CTCG

TTG

TATC

TGG

12CO

NCA

TGAG

CATG

GTG

ATG

TCTR

I12

Conv

entio

nalP

CRPa

squa

liet

al.(

2011

);W

ard

etal

.(20

02)

Deox

yniva

leno

l-pro

ducin

gst

rain

12-3

FCT

TTG

GCA

AGCC

CGTG

CA12

CON

CATG

AGCA

TGG

TGAT

GTC

TRI1

2Co

nven

tiona

lPCR

Pasq

uali

etal

.(20

11);

War

det

al.(

2002

)

Niva

leno

l-pro

ducin

gst

rain

Tri1

3P1

CTCS

ACCG

CATC

GAA

GAS

TCTC

Tri1

3P2

GAA

SGTC

GCA

RGAC

CTTG

TTTC

TRI1

3Co

nven

tiona

lPCR

Pasq

uali

etal

.(20

11);

Wan

get

al.(

2008

)

3-AD

ON

-pro

ducin

gst

rain

s3A

DO

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Key factors in the development of FRR are the previous crop,residue management, nitrogen fertilization, plant density and theenvironmental conditions. Conidial germination and germ tubeextension on sterile and unsterile wheat straw leaf sheaths weresignificantly higher relative to other crop residue colonizers, suchas Gliocladium, Trichoderma and Penicillium spp., when tested atdifferent water potential ¥ temperature (Magan, 1988). Therefore,wheat monoculture and/or rotation with another cereal crop (suchas barley, triticale, rye, spelt, oat or corn) boosts the inoculum and,consequently, the chances of increasing FRR severity: althoughcereals are not equally sensitive to F. culmorum, all may contrib-ute to maintain inoculum survival in the soil. High nitrogen ferti-lization rates and high sowing density are believed to increase theincidence of FRR: increased leaf index and transpiration rates andthe reduction of plant water potential induce water stress and,consequently, a higher sensitivity to the pathogen (Davis et al.,2009; Papendick and Cook, 1974).

FRR by F. culmorum is severe when wheat is grown in warmareas, where the host plant is more subject to water stress(Bateman, 1993; Cariddi and Catalano, 1990; Chekali et al., 2010;Colhoun et al., 1968; Inglis and Cook, 1986; Papendick and Cook,1974; Parry, 1990; Prew et al., 1995). Drought conditions increasethe susceptibility of the plant rather than the virulence of thefungus. However, FHB occurs preferentially when the pathogen ispresent at the soil level, and the weather is moist and warm, withfrequent rains between flowering and kernel filling stages(Bateman, 2005). Rain is an essential determinant of FHB infection,as demonstrated experimentally on wheat crops receiving over-head irrigation (Strausbaugh and Maloy, 1986). The macroconidiathat are found in soil on crop residues reach the ear by rain splash,wind or insects, attaining distances of up to 60 cm vertically and1 m horizontally (Jenkinson and Parry, 1994; Parry et al., 1995;Rossi et al., 2002). Compared with F. graminearum, F. culmorumdoes not produce ascospores, being unable to differentiate sexual

perithecia. From an epidemiological standpoint, this is paramount,given the crucial role of wind-borne ascospores in the spread ofFHB caused by the former species (Markell and Francl, 2003).

Once the inoculum reaches the ear, humidity and temperaturein the crop microclimate play a critical role: it takes at least 24 h ofmoisture with temperatures above 15 °C, with an optimum of25 °C, to allow infection (Doohan et al., 2003; Parry et al., 1995).Nonetheless, among the species causing FHB, F. culmorum has thesmallest need for the presence of high relative humidity to infectwheat (Klix et al., 2008; Rossi et al., 2001).

POPULATION DIVERSITY ANDMYCOTOXIN PRODUCTION

The perfect stage (teleomorph) of F. culmorum is not known, eventhough transcribed mating type genes have been identified in thisspecies. Only one MAT idiomorph (MAT1-1 or MAT1-2) has beenreported so far, postulating heterothallism (Kerényi et al., 2004;Mishra et al., 2003; Obanor et al., 2010; Tòth et al., 2004). It isnoteworthy that, among a vast majority of isolates from Turkeycarrying either the MAT-1 or MAT-2 sequence, Çepni et al. (2012)were recently able to identify two F. culmorum isolates thatcarried both sequences.

The genetic variability of F. culmorum in different geographicalareas suggests that genetic exchange occurs or has occurred in thepast, as the population structure is not clonal (Miedaner et al.,2001; Mishra et al., 2003; Tòth et al., 2004).

Population studies carried out within restricted geographicalareas, or even at the single field level, have reported a widegenetic variability, whereas relatively modest differences havebeen detected among populations obtained from different climaticregions (Gargouri et al., 2003; Nicholson et al., 1993). A high levelof diversity has also been found recently in F. culmorum isolatesfrom Turkey by intergenic spacer-restriction fragment length poly-morphism (IGS-RFLP) analysis, further confirming the wide geneticvariability associated with FRR disease (Çepni et al., 2012). Aphylogenetic study conducted with over 100 isolates of F. culmo-rum from Australia, West Asia, North Africa and Europe identifiedthree to four distinct groups or lineages. However, no correlationwas found between lineages and their geographical origin, withthe exception of one cluster including isolates from a single area(Obanor et al., 2010).

Two chemotypes have been described in F. culmorum: chemo-type I, which produces deoxynivalenol (DON) and/or its acetylatedderivatives (3-ADON, 15-ADON), and chemotype II, which pro-duces nivalenol (NIV) and/or fusarenone-X (FUS), NIV being 10times more toxic than DON (Minervini et al., 2004). DNA sequencevariation in the coding region of the trichothecene biosyntheticgene TRI8 was found in Fusarium spp., including F. culmorum,indicating that differential activity of the Tri8 protein (i.e.deacetylation of the trichothecene biosynthetic intermediate 3,15-

Table 2 Non-polymerase chain reaction (PCR)-based approaches todiscriminate and detect Fusarium culmorum.

Technology employed Reference

Surface plasmon resonance (SPR) sensorbased on DNA hybridization

Zezza et al. (2006)

Luminex assay to discriminate Fusariumspecies and chemotypes

Ward et al. (2008)

DNA microarray for detection andidentification of 14 Fusarium species

Kristensen et al. (2007)

Spore shape discrimination analysed bycomputerized algorithms

Dubos et al. (2012)

Metabolomic analysis and monitoring of themetabolic activity

Lowe et al. (2010)

Electronic nose for discriminating speciesinfecting grains

Eifler et al. (2011)

Quick matrix-assisted laserdesorption/ionization (MALDI) lineartime-of-flight mass spectrometry analysisof fungal spores

Kemptner et al. (2009)



diacetyldeoxynivalenol at carbon 15 versus carbon 3 to yield3-ADON or 15-ADON, respectively) determines the 3-ADON and15-ADON subchemotypes in Fusarium (Alexander et al., 2011).

Studies on F. culmorum chemotypes are less frequent thanthose focusing on F. graminearum, but it is possible to trace theirdistribution in some geographical areas (Table 3).

The link between the presence of the pathogen and its toxins (inthis case, type B trichothecenes) is often complicated by the com-plexity of toxin induction and pathogen adaptation. AlthoughF. culmorum has been reported to be one of the main fungalspecies associated with diseased wheat in warmer regions, suchas Turkey (Tunalı et al., 2006), Tunisia (Kammoun et al., 2010),

A B

E

C

D Fig. 1 Foot and root rot (FRR) symptoms: (A) macroconidia; (B) browning on the stem base; (C) reddish-pink discoloration on the basal nodes; (D,E) presence ofwhiteheads.



Australia and New Zealand (Lauren et al., 1992), no clear data onits role in toxin accumulation are evident. Moreover, although thisspecies was the most prevalent in 2009 in the central region ofPoland, the level of toxin contamination reported in the grains wasvery low, and no direct correlation between fungal contaminationand toxin accumulation could be found (Chelkowski et al., 2012).The identification of the chemotype may provide insight into the

toxigenic potential of F. culmorum isolates. For example, the pres-ence of F. culmorum with the NIV subchemotype has been linkedto the accumulation of NIV in wheat harvested in Luxembourgduring 2007 and 2008 (Pasquali et al., 2010), confirming the find-ings obtained in a within-field comparison experiment describedby Xu et al. (2008). Similar results pinpointing a role of F. culmo-rum in the accumulation of NIV have been reported in a recent

A B

F E

C

D Fig. 2 Fusarium head blight (FHB) symptoms: (A,B) head blight symptoms; (C) brown/purplish discoloration below head; (D–F) orange sporodochia on spikelets.



screening of historical Danish seed samples by real-time PCR(Nielsen et al., 2012).

HOST–PATHOGEN INTERACTION

Although a wide array of information on F. culmorum pathogen-esis can be inferred from reports using F. graminearum as thespecies of interest, in the present review, we have attempted tolimit references to related Fusarium species only when absolutelynecessary. Fusarium culmorum remains viable as mycelium in cropresidues left on the ground surface, and can survive in soil for2–4 years by forming chlamydospores (Bateman et al., 1998;Cook, 1980; Inglis and Cook, 1986). When the seed germinates,the fungus penetrates through the lesions that are formed duringprimary root emergence, and then progresses towards the culm.Alternatively, it penetrates through the stomata at the insertionpoint of the basal leaf sheath towards the stem. The colonizationfollows, initially, an intercellular apoplastic pathway between cellsof the epidermis and cortex; subsequently, the fungus progressesintracellularly in the symplast to complete colonization of thetissues (Beccari et al., 2011; Covarelli et al., 2012; Pettitt and Parry,2001).The fungus may then grow further along the stem, althoughit is usually limited to the first basal internodes. The symptoms of

basal browning may occur prior to the presence of the fungus inthese portions, as a result of the plant response to infection(Beccari et al., 2011; Covarelli et al., 2012).

FHB infection occurs between flowering and the soft doughstage (GS 65–85; Zadoks’ scale modified by Tottman andMakepeace, 1979), the phases between flowering and the milkstage (GS 65–77) being the most favourable for the infection byF. culmorum (Lacey et al., 1999). Once the macroconidia arriveonto the ear, they germinate rapidly and the fungus penetratesinto host tissues, either directly through the stomata, or throughthe floret mouth or crevices formed between the palea andlemma, and then progresses inter- and intracellularly and reachesthe endosperm within 12–24 h. Betaine and choline, which arecontained in the anthers, stimulate the growth of conidial germtubes towards the head surface (Strange et al., 1974, 1978).Similar to other FHB pathogens, F. culmorum may have an initialbrief biotrophic phase within plant tissues, but then shifts to anecrotrophic stage through the production of trichothecenes andcell wall-degrading enzymes (CWDEs; Bushnell et al., 2003).

The infection process by F. culmorum is strongly influenced bytemperature, humidity, carbon and nitrogen availability, as well asthe ability of the specific strain to produce mycotoxins that mayconfer a higher aggressiveness by inhibiting the defence response

Table 3 Distribution of Fusarium culmorum chemotypes: country, chemotyping method used, number of isolates analysed, main finding and bibliographic reference.

CountryChemotypingmethod used

Number ofisolates analysed Main finding Reference

Europe Chemical 42 ~84% DON producers, ~16% NIV producers Gang et al. (1998)Germany Chemical 27 ~60% NIV producers, ~40% DON producers Muthomi et al. (2000)Norway Chemical 23 Mostly 3-ADON producers, two NIV producers Langseth et al. (2001)France Genetic and chemical 60 58% NIV producers, 42% DON producers Bakan et al. (2001, 2002)Denmark, Germany, Austria Chemical 102 1995 sampling: ~90% DON producers, ~10%

NIV producersHestbjerg et al. (2002)

The Netherlands Genetic 85 2000–2001 sampling: mostly NIV producers Waalwijk et al. (2003)Worldwide (Australia, Canada,

Israel, Hungary, Germany,Denmark, the Netherlands,Morocco)

Genetic and chemical 37 19% NIV producers, 81% 3-ADON producers Tòth et al. (2004)

UK Genetic 157 DON producers are prevalent, but NIV producersare distributed consistently

Jennings et al. (2004)

Europe (Spain, Italy, Poland,Norway, the Netherlands,France, Finland, formerYugoslavia)

Genetic 55 ~20% NIV producers, ~80% 3-ADON producers Quarta et al. (2005)

Belgium Genetic 128 In 2007 (95%) and in 2008 (88%) NIVproducers are the most diffused

Audenaert et al. (2009)

Luxembourg Genetic and chemical 175 3-ADON and NIV producers are evenlydistributed

Chemotyping is useful to predict toxin contentChemical analysis confirms genetic chemotyping

Pasquali et al. (2010)

Tunisia Genetic and chemical 100 Mostly 3-ADON producers, 2% NIV producersChemical analysis confirms genetic chemotyping

Kammoun et al. (2010)

Poland Genetic 68 6% NIV producers, 94% 3-ADON producers Baturo-Ciesniewska andSuchorzynska (2011)

Turkey Genetic 21 100% 3-ADON producers Yörük and Albayrak (2012)

ADON, acetylated deoxynivalenol; DON, deoxynivalenol; NIV, nivalenol.



by the plant. Key factors for its growth are temperature and wateravailability (water activity aw; Magan et al., 2006). Schmidt-Heydtet al. (2011) compared the effect of aw ¥ temperature of oneisolate of F. culmorum and F. graminearum on growth, F. culmo-rum showing an optimum at 30 °C and 0.98aw, whereas itsminimum limit for growth was 15 °C over 0.88–0.995aw. Germi-nation of F. culmorum macroconidia is restricted to a minimum of0.86aw, but is functional over a wide temperature range from 5to 35 °C (Magan et al., 2006). Fusarium culmorum hydrolyticenzymes are produced over the same broad temperature range,allowing the rapid utilization of nutritional resources (Magan andLynch, 1986).

Mycotoxin biosynthesis is mainly influenced by temperatureand moisture (Homdork et al., 2000; Tanaka et al., 1988). Studieswith F. culmorum and F. graminearum isolates from Spain(Llorens et al., 2004) showed that both fungi require high humidity(>0.90aw) to support trichothecene production, with optimumtemperatures of 25–28 °C for DON, 20 °C for NIV and a minimumof 15 °C for 3-ADON. Fusarium culmorum demonstrated a signifi-cantly higher mycotoxigenic rate (up to five times higher for typeB trichothecenes) than F. graminearum, and the toxin biosynthesiscould not be correlated with mycelial growth (Llorens et al., 2004;Lori et al., 1999).

Trichothecene production, which is driven by the expression ofthe TRI5 gene encoding the key biosynthesis enzyme trichodienesynthase, can be observed as early as 36 h post-inoculation duringthe colonization of wheat spikelets (Beccari et al., 2011; Kang andBuchenauer, 2002).The ability of aggressive strains of F. culmorumto infect wheat is related to their ability to produce larger amountsof DON in culture or in infected tissues (Hestbjerg et al., 2002;Manka et al., 1985; Scherm et al., 2011), although correlation isnot always linear (Gang et al., 1998). Similar to F. graminearum,trichothecene mycotoxins produced by F. culmorum are essentialfor the spread of the disease by inhibiting defence mechanismsactivated by the plant (Wagacha and Muthomi, 2007). Followinginoculation of the stem base of soft wheat seedlings with F. cul-morum, Covarelli et al. (2012) demonstrated the translocation ofDON to the head, even though the fungus was unable to growsystemically beyond the third node. This finding suggests that FRRmay represent an additional potential source of grain contamina-tion, providing an explanation for previous reports on the pres-ence of DON in grain harvested in the field, even in the absence ofdetectable fungus (Xu et al., 2008).

Different plant compounds involved in host–pathogen interac-tions are able to interfere with mycotoxin production within planttissue (Boutigny et al., 2008). On infection, plant cells respondwith a hypersensitive reaction by the generation of reactiveoxygen species (ROS), such as H2O2 and superoxide. The strongoxidative properties of H2O2 modulate trichothecene biosynthesis(Ponts et al., 2006; Sweeney and Dobson, 1999), leading toincreased expression of TRI genes (Ochiai et al., 2007; Ponts et al.,

2007). In vitro production of DON and ADON by F. culmorumchemotype I isolates was enhanced after H2O2 treatment, whereasNIV and FUS production by chemotype II isolates was reduced(Ponts et al., 2009). Differences in the efficiencies of detoxificationhave been described in F. culmorum isolates of the two chemo-types. Usually, chemotype I isolates exposed to oxidative stressreact with an increase in catalase activity, resulting in a higherH2O2-destroying capacity (Ponts et al., 2009).

Typical growth patterns of F. culmorum are accompanied by apH increase during infection (Lamour and Marchant, 1977), fol-lowed by increased extracellular enzyme expression activity andDON production. The role of CWDEs as virulence factors in F. cul-morum has been investigated extensively (Cooper et al., 1988;Hestbjerg et al., 2002; Miedaner et al., 1997; Tunalı et al., 2012;Wang et al., 2006). The production of CWDEs able to hydrolysecellulose, xylan and pectin of the plant cell wall (PCW) allowsF. culmorum to invade host tissues within 3–4 days (Kang andBuchenauer, 2002). These alterations may occur even before thepresence of fungal hyphae within the host tissues, suggesting anapoplastic movement of these enzymes (Kang and Buchenauer,2000a, 2000b).

Fusarium culmorum creates the conditions for maximum activ-ity of its pectin lyases (PNLs) and other depolymerizing enzymesby raising the apoplastic pH from 6 to 7.3. When grown withpectin as the sole carbon source, F. culmorum modulates the pH tomore alkaline conditions, favouring significantly PNL productionand repressing polygalacturonase (PG) expression, which has anactivity window at the very initial stages of infection. This pHchange triggers the synthesis of additional ‘weapons’, such assubtilisin and trypsin-like enzymes, which are relevant in thiscolonization phase (Aleandri et al., 2007; Pekkarinen and Jones,2002; Pekkarinen et al., 2002). In vivo, F. culmorum attacks anarabinoxylan-rich cell wall (constituting up to 40% of its compo-nents) of graminaceous crops, and produces much more xylanasesthan other pathogens (Bëlien et al., 2006; Carpita, 1996; Hatschet al., 2006). Moreover, effective hydrolysis of PCW requires thesynergistic action of several CWDEs that have been found to beexpressed and to act in complexes (Alfonso et al., 1995; Collinset al., 2005; Jaroszuk-Scisel et al., 2011). The activities of sevenCWDEs (glucanases, chitinases, xylanases, endo- and exocellu-lases, pectinases, PGs) have been traced in cultures of F. culmorumgrown on fungal cell walls (FCWs) or PCW as carbon source, withglucanases, chitinases, xylanases and pectinases revealing a sig-nificantly higher activity. Replacement of FCW by PCW triggers anincrease in PG activity, underlining their role in the initial phase ofhost cell wall attack (Jaroszuk-Scisel and Kurek, 2012). Fusariumculmorum cultures with FCW as the only carbon source enhancetheir acid glucanase and chitinase repertoire, whereas PCW-basedcultures produce high concentrations of xylanases, as also docu-mented for Fusarium-infected barley (Jaroszuk-Scisel and Kurek,2012; Schwarz et al., 2002). Differences in the disease induction



and tissue colonization between pathogenic and nonpathogenicisolates of F. culmorum have also been related to their differentCWDE efficiencies (Jaroszuk-Scisel and Kurek, 2012) and to theirability to induce local and systemic defence responses, i.e. cell wallthickening or oxidative burst (Jaroszuk-Scisel et al., 2008; Mar-tinez et al., 2000).

On infection with an F. culmorum spore suspension, wheatseeds and seedlings express several pathogenesis-related (PR)proteins, including glucanases (PR1, PR2), chitinase (PR3), peroxi-dase (POX) and the PR protein Wheatwin1-2 (PR4) (Aleandri et al.,2008; Bertini et al., 2003; Caruso et al., 1999). In in vitro experi-ments, stimulation of wheat seeds with different chemical induc-ers, such as salicylic acid (SA) and jasmonic acid (JA), or bymechanical damage through wounding, was followed in eachcase by an increase in PR4 expression, indicating its regulation bythese pathways (Bertini et al., 2003). Fusarium culmorum-infectedwheat roots, instead, underwent increased expression of defence-associated genes in leaf sheaths which had not yet been in contactwith the fungus, indicating the role of a systemic response in FRR(Beccari et al., 2011).

Effective and persistent resistance in the host plant can beinduced by low-molecular-mass molecules able to restrict fungalgrowth in the different tissue layers or by the inhibition of fungalCWDEs. In wheat, xylanase-specific inhibitors, such as TAXI (Goe-saert et al., 2003), XIP (Juge et al., 2004), thaumatin-like XI (TLXI;Fierens et al., 2007) and PG-inhibiting proteins (PGIPs; Di Matteoet al., 2003; Ferrari et al., 2012) have been described. Transgenicwheat plants expressing the bean PvPGIP2 gene in their flowersshowed significantly reduced symptoms in F. graminearum-incitedFHB (Ferrari et al., 2012). Pectin methyl-esterification influencesplant resistance, as PCW becomes less susceptible to fungal pec-tinases and endopolygalacturonases. The level of esterification inthe PCW is controlled by a pectin methyl-esterase inhibitor (PMEI),supposed to confer resistance to the plant when demethylation iseffectively inhibited. Wheat transgenic lines expressing AcPMEIfrom Actinidia chinensis showed reduced pectin methyl-esterase(PME) activity, and hence high pectin methylation levels and sig-nificantly reduced disease symptoms following inoculation withF. graminearum (Volpi et al., 2011). Recently, three PMEI geneshave been identified and characterized in wheat (Rocchi et al.,2012), opening up new perspectives in the development of trans-genic wheat lines potentially resistant to different Fusariumspecies, including F. culmorum.

Plants are able to chemically transform trichothecenes by theirdegradation or detoxification, or to reduce their accumulation bythe inhibition of biosynthesis through the activity of endogenouscompounds (Alabouvette et al., 2009; Bollina and Kushalappa,2011; Boutigny et al., 2010; Yoshinari et al., 2008). Glycosylationrepresents the main plant-driven chemical transformation ofmycotoxins in response to Fusarium attack (Karlovsky, 2011). Inthe naturally FHB-resistant wheat cultivar Sumai3, genetic

mapping has revealed that the ability to detoxify DON by a DONglucosyltransferase colocalizes with a major quantitative traitlocus (QTL) for FHB resistance (Lemmens et al., 2005). TransgenicArabidopsis thaliana expressing a barley UDP-glucosyltransferaseexhibited resistance to DON (Shin et al., 2012). Although severalstudies have been devoted to the selection of plant glycosylases,this does not appear to be an efficient strategy to control myco-toxin production, because of the possibility that glycosyl-protectedmycotoxins may be re-converted into the original toxic form byhydrolysis in the digestive tract or during food/feed processing(the so-called ‘masked’ mycotoxins).

Some secondary plant metabolites, present in larger amounts inFHB-resistant plants, have been shown to inhibit fungal growthin vitro and/or mycotoxin production by Fusarium spp. Theseare phenolic and polyphenolic compounds belonging to thebenzoic and cinnamic acids, furanocoumarins, phenylpropanoids,chromenes and flavones (Bakan et al., 2003; Boutigny et al., 2010;Mellon et al., 2012; Ojala et al., 2000; Takahashi-Ando et al.,2008; Wu et al., 2008). Most are constituents of PCW: in responseto infection, plants release phenols from the cell wall in order tolimit the pathogen spread by reinforcing plant structural compo-nents. Some dialkyl resorcinols and coumarins manifest antifungalactivity against F. culmorum (Ojala et al., 2000; Pohanka et al.,2006). Moreover, phenols present anti-oxidant and/or radical scav-enging activities (Kim et al., 2006). Therefore, defence mecha-nisms triggered in the plant in response to pathogenic oxidativeprocesses involve the production of these secondary metabolitesthat can interfere in different ways with trichothecenebiosynthesis.

OPTIONS FOR CONTROL

The multiple factors influencing fungal growth and trichotheceneproduction by F. culmorum require the application of an inte-grated pest management approach, combining genetic, agro-nomic, chemical and biological control measures.

The growth of susceptible wheat varieties does not onlyincrease the severity of FHB, but also the fungal biomass, with aconsequent increase in the amount of toxins present in the har-vested grain (Blandino et al., 2012; Snijders and Krechting, 1992;Tòth et al., 2008). The adoption of wheat cultivars showing resist-ance to primary infection and to the spread of the disease wouldbe the ideal strategy. Unfortunately, there are no highly resistantwheat cultivars (Pereyra et al., 2004; Wisniewska and Kowalczyk,2005). Nonetheless, extensive effort has been devoted to map theQTLs associated with FHB resistance in wheat (see, for example,Häberle et al., 2009; Schmolke et al., 2008). Genotypes bearingresistance to FHB have been reported and it is encouraging thatresistance of a given genotype is not specific to a single Fusariumspecies, but can be extended to all the causative agents of thisdisease (Mesterhazy et al., 2005; Miedaner et al., 2012).



Being a typical seed-borne pathogen, F. culmorum survives onor within the infected seed, which remains the main cause of pre-or post-emergence seedling death, and contributes to increase theinoculum potential in the soil. Consequently, ploughing should bepreferred to direct sowing or minimum tillage practices, whichfavour inoculum survival (Blandino et al., 2012; Dill-Macky andJones, 2000; Miller et al., 1998; Teich and Nelson, 1984). Similarly,crop rotation with noncereal host crop intermediates, such aslegumes, alfalfa and Brassicaceae, may reduce the incidence ofdisease (Kurowski et al., 2011; Parry et al., 1995). The use ofhealthy seed coated with fungicides represents a most efficientmeans of control, but is usually limited to the early stages of thewheat cycle, as fungicides do not maintain their efficiency over alonger period. To improve the slow release of the delivered com-pound, a tebuconazole–b-cyclodextrin inclusion complex hasbeen proposed for the control of FRR during the early stages ofdurum wheat growth (Balmas et al., 2006).

Several fungicides, mainly belonging to the azole (bromucona-zole, cyproconazole, metconazole, prochloraz, propiconazole,prothioconazole and tebuconazole) and strobin (azoxystrobin)classes, have been shown to control the disease by up to 70% inthe field and to reduce the amount of mycotoxins in kernels; thisis particularly evident under low disease pressure or on wheatgenotypes possessing moderate resistance (Chala et al., 2003;Jones, 2000; Menniti et al., 2003; Paul et al., 2008). However, anincrease in mycotoxin content in the kernel can occur when fun-gicides are applied at sublethal concentration or if they differ intheir activity against distinct Fusarium pathogens (Covarelli et al.,2004; Gardiner et al., 2009; Gareis and Ceynowa, 1994; Haidu-kowski et al., 2005; Hysek et al., 2005; Matthies and Buchenauer,2000; Matthies et al., 1999; Ochiai et al., 2007; Simpson et al.,2001; Stack, 2000). Moreover, the prolonged use of moleculessharing the same mode of action may induce a selective pressureon the pathogenic fungal populations, enabling the selection ofresistance traits. Resistance to trifloxystrobin (a complex III respi-ration inhibitor) and isopyrazam (a complex II respiration inhibi-tor) has been reported recently on two isolates within twodifferent chemotypes (Pasquali et al., submitted). These resultshave been confirmed on a larger set of isolates collected in Lux-embourg (M. Beyer, Centre de Recherche—Gabriel Lippmann,Belvaux, Luxembourg , personal communication), suggesting that,as in the case of F. graminearum, these resistance traits are ofnatural origin (Dubos et al., 2011, 2013).

An alternative approach to minimize the risk of resistance amongfungal populations relies on the use of new molecules, based onthe structure of natural and natural-like inhibitors, able to counter-act the pathogenic and mycotoxigenic potential of natural popula-tions of Fusarium, rather than acting on their saprophytic phase, orcapable of stimulating natural resistance responses by the hostplant. Essential oils of plant origin and some natural monoterpenes,considered as ‘Generally Recognized As Safe’ (GRAS) chemicals

(safe for food use), have both inhibitory effects against mycotoxinbiosynthesis and fungicide activity (Dambolena et al., 2008;Ellouzeet al., 2012;Yaguchi et al., 2009). In particular, extracts from malva,chamomile and citrus manifest fungistatic activity againstF. culmorum (Ellouze et al., 2012; Magro et al., 2006).

A specific and powerful inhibitory activity has been demon-strated by phenolic and polyphenolic natural compounds (Bakanet al., 2003; Boutigny et al., 2010; Desjardins et al., 1988;Takahashi-Ando et al., 2008). The most abundant phenolsextracted from maize kernel pericarp and wheat bran are trans-ferulic acid and the corresponding dehydrodimers (DFAs), namelydehydrodiferulates (Bily et al., 2003; Boutigny et al., 2008; Kimet al., 2006). Hydroxycinnamic acids are known to be major com-ponents of the primary cell wall of cereals (Bakan et al., 2003).These compounds are ester bound to the C5 hydroxyl of thearabinosyl side chain of cell wall arabinoxylan chains. The feruloylresidues, predominant species, can also be dimerized under anoxidative coupling mediated by POXs, form cross-links or dehy-drodimers of ferulic acid, and then lead to a reinforcement of theprimary wall of the plant.

A phenolic fraction rich in these phenolic acids manifested adrastic reduction on in vitro DON and ADON biosynthesis by F. cul-morum (Boutigny et al., 2010). Although the mechanism remainsunclear, it is reasonable to hypothesize that these compounds,mainly DFAs, interfere with in vitro cell wall degradation by fungalhydrolases. The activity of fungal esterases, overexpressed duringgrowth on host tissues, can release free forms of ferulic ester fromcell wall tissues (Balcerzak et al., 2012; Jaroszuk-Scisel et al.,2011). Once released, free ferulate may inhibit the ability ofFusarium to produce mycotoxins. One of the DFAs present in thephenolic acid mixture, 8,5′-benzofuran dimer, shows the sameinhibitory activity of ferulic acid against F. culmorum, although asynergism of the phenolic acid mixture may play a crucial role inthe inhibition of mycotoxins (Boutigny et al., 2010).

The X-ray crystal structure of trichodiene synthase, purified fromF. sporotrichioides and complexed with Mg2+(three ions)-inorganic pyrophosphate (PPi), provides critical details regardingthe molecular recognition of PPi, giving further insights into thetrichothecene pathway, and therefore on the possibility of usingexternal ligands able to interfere with mycotoxin production(Rynkiewicz et al., 2001; Vedula et al., 2008). The combination ofbioprospecting and computational studies offers a useful way toselect and investigate new natural and natural-like mycotoxininhibitors and fungicides against Fusarium. A collection of naturaland natural-like phenols and dimers was recently correlated withtheir ability to inhibit in vitro 3-ADON and DON in F. culmorumand to interact with the trichodiene synthase crystal structure (G.Delogu, Istituto CNR di Chimica Biomolecolare, Sassari, Italy,unpublished data).

The susceptibility of the model plant A. thaliana to bothF. graminearum and F. culmorum infection (Urban et al., 2002)



has opened up new possibilities of developing high-throughputexperimental approaches to select new protecting compounds.Working with F. graminearum, Schreiber et al. (2011) identifiedsmall molecules, such as sulphamethoxazole and the indolealkaloid gramine, that protect Arabidopsis seedlings from infec-tion. The same chemicals reduced significantly the severity ofF. graminearum infection in wheat (Schreiber et al., 2011).

The integration of biological control approaches may offer aneffective support to F. culmorum management on wheat andother cereals. The flag leaf and ripening ear surfaces of wheat arecolonized by a panoply of micro-organisms whose numbers mayvary with plant growth stage and environmental conditions(Magan and Lacey, 1986). The application of natural antagoniststo the crop residues or directly onto plant organs by spray or byseed dressing achieved reduced severity of FRR or FHB by F. cul-morum on wheat, and the contamination of grain with mycotoxins(Table 4).

FUNCTIONAL GENOMICS

The F. culmorum genome is largely unknown. On analysis of theNational Center for Biotechnology Information (NCBI) databasefor proteins associated with F. culmorum, 189 hits were returnedon 15 November 2012. Annotated proteins include elongationfactor 1a, a putative reductase, the RNA polymerase II, a phos-phate permease, a putative regulatory protein used for phyloge-netic analysis (Ward et al., 2002) and genes of the TRI cluster,involved in the synthesis of trichothecenes, also used for phyloge-

netic studies. Other F. culmorum annotated proteins include anABC transporter (Skov et al., 2004), the trichodiene synthase usedfor RNA silencing experiments (Scherm et al., 2011), three puta-tive allergenic proteins (Hoff et al., 2003), hydrophobin precursorsinvolved in gushing (Stübner et al., 2010) and further proteinsinvolved in the foam effect in beers (Zapf et al., 2007), and afragment of a polyketide synthase essential in zearalenone bio-synthesis (Atoui et al., 2012). Other genes have also been clonedin F. culmorum whilst studying the production of secondarymetabolites, such as the nonribosomal peptide synthetase NPS2able to synthesize ferricrocin (Tobiasen et al., 2007). Proteinaseshave also been isolated from F. culmorum (Levleva et al., 2006).

Functional characterization of the genes involved in the patho-genic process in F. culmorum is even more limited. Genetic trans-formation of the fungus is well established (Doohan et al., 1998),but the lack of a full genome has limited the functional analysis ofgenes to a few examples. Scherm et al. (2011) demonstrated thatRNAi silencing as a functional approach is working in F. culmo-rum. Silencing of the zinc finger transcription factor TRI6, usinginverted repeat transgenes, led to significantly decreased expres-sion rates of the trichodiene synthase encoding gene TRI5and, consequently, to a decline in DON production. Hence, tri-chothecene production of F. culmorum is tightly related to itsaggressiveness and virulence in determining the symptoms of FRRon wheat (Scherm et al., 2011).

A second gene shown to play a role in pathogenesis is an ABCtransporter, FcABC1, supposed to confer resistance to defensivecompounds produced by the plant during the head infection

Table 4 Biological control agents developed to control Fusarium culmorum infection on wheat.

Antagonist Target disease Application method Reference

Chaetomium sp.Idriella bolleyiGliocladium roseum

FRR Seed coating (field) Knudsen et al. (1995)

Alternaria alternataBotrytis cinereaCladosporium herbarum

FHB Spray at ear emergence complete oranthesis complete (glasshouse)

Liggitt et al. (1997)

Trichoderma harzianum FRR Seed coating (field) Michalikova and Michrina (1997)Trichoderma harzianumTrichoderma atrovirideTrichoderma longibrachiatumGliocladium roseumPenicillium frequentans

FRR, FHB Seed coating (field) Roberti et al. (2000)

Gliocladium roseum(Clonostachys rosea)

FRRFRR

Seed coating (field)Seed coating (in vitro)

Jensen et al. (2000);Roberti et al. (2008)

Phoma betae FHB Spray at early anthesis (glasshouse) Diamond and Cooke (2003)Pseudomonas fluorescensPantoea agglomerans

FRR Seed coating (glasshouse and field) Johansson et al. (2003)

Fusarium equiseti FHB Spray at anthesis (field) Dawson et al. (2004)Bacillus mycoides FRR Seed coating (microplot) Czaban et al. (2004)Different filamentous fungi and yeasts FRR, FHB Wheat straw (in vitro) Luongo et al. (2005)Pseudomonas fluorescensPseudomonas frederiksbergensis

FHB Spray at mid-anthesis (glasshouseand field)

Khan and Doohan (2009);Petti et al. (2008)

Streptomyces sp. FRR Seed coating (glasshouse) Orakci et al. (2010)Bacillus subtilis FRR Seed coating (glasshouse) Khezri et al. (2011)Trichoderma gamsii FRR, FHB Wheat haulms and rice kernels (in vitro) Matarese et al. (2012)



process in wheat (Skov et al., 2004). The FcABC1 deletion mutantwas unaltered in its physiology, but showed up to 98% reducedaggressiveness compared with the wild-type strain, suggestingthat the ability to excrete secondary plant metabolites allowsF. culmorum to overcome the inhibition of host tissue invasion(Skov et al., 2004).

An F. culmorum topoisomerase I gene (top1) was found by arandom plasmid insertional mutagenesis approach in F. gramine-arum and deleted in F. culmorum (Baldwin et al., 2010). The dele-tion mutant showed a complete block of conidia production asa result of its inability to regulate the transcriptional changesrequired for perithecial development. Furthermore, the mutantshowed a significantly reduced virulence in wheat ear infectionwith low ability to colonize tissues after penetration (Baldwinet al., 2010).

The role of the gene FcStuA, a stuA orthologue protein with anAPSES domain sharing 98.5% homology to the FgStuA transcrip-tion factor (FGSG10129) of F. graminearum (Lysøe et al., 2011),was recently determined by the functional characterization ofdeletion mutants. FcStuA was found to completely control patho-genicity and to reduce significantly (but not by blocking as inF. graminearum) DON production in F. culmorum mutants, toge-ther with a strong impairment of conidiation and significant mor-phological changes (M. Pasquali, Centre de Recherche—GabrielLippmann, Belvaux, Luxembourg, personal communication).

Given the very limited number of genes described to beinvolved in the pathogenic process in F. culmorum, further instru-ments and approaches are needed to explore the pathogenicarsenal of the fungus. A forward genetic tool based on a transpo-son insertion screening in the genome of F. culmorum (Spanuet al., 2012) did not lead to the identification of FRR PR genes, butallowed the isolation of partial sequences of aurofusarin genesand other genes involved in oxidative stress resistance, and thepartial mapping of this unknown genome by the generation ofmore than 50 000 bp of F. culmorum sequence.

The availability of genomes would facilitate targeted functionalgenomics studies that, at the moment, are based on the similari-ties of genes with F. graminearum (Baldwin et al., 2010), but thiscannot explore genes that are peculiar to F. culmorum (Spanuet al., 2012).

It is quite opportune that two F. culmorum genome sequencingprogrammes are on their way to being released. The first involvesF. culmorum isolate FcUK99 (NRRL 54111; FGSC 10436), recov-ered from an infected wheat ear in the UK in 1998 (Baldwin et al.,2010). This isolate is fully pathogenic on wheat ears, tomato fruitsand Arabidopsis floral tissue, and produces DON and 3-ADON. By454 sequencing, a 13.4¥ coverage of the F. culmorum isolateFcUK99 genome has been generated. In addition, four normalizedcDNA libraries have been Illumina sequenced to give a transcrip-tome coverage of 100¥ (6 Gb of data). The F. culmorum genomesize is estimated to be 39 Mbp, i.e. slightly larger than F. gramine-

arum. In addition, the draft genomes of a further three F. culmo-rum isolates with different biological properties have beengenerated by sequencing with Illumina technology using 100-bppair-end reads (M. Urban, J. Antoniw, N. Hall and K. E. Hammond-Kosack, Wheat Pathogenomics, Plant Biology and Crop SciencesDepartment, Rothamsted Research, Harpenden, Herts, UK, per-sonal communication).

As part of a larger programme of sequencing of the genomes ofcereal Fusarium pathogens causing crown rot disease using Illu-mina paired-end sequencing (see Gardiner et al., 2012), DonaldGardiner and John Manners at the Commonwealth Scientific andIndustrial Research Organization (CSIRO, Clayton, Vic., Australia),together with Bioplatforms Australia (Sydney, NSW, Australia),have obtained sequence information for another isolate of F. cul-morum, obtained from infected crown tissue of a wheat plantgrown in Western Australia. Genome coverage will be >30-foldand sequence information will be made publicly available early in2013 on an Australian-based website, and ultimately published onthe NCBI site (J. M. Manners, CSIRO, Clayton, Vic., Australia, per-sonal communication).

FUTURE CHALLENGES

Although it is not yet regarded as a ‘model system’, theF. culmorum–wheat interaction presents several features allowingit to be considered as a tractable model for investigation. Sequenc-ing data permit a comparison of F. culmorum with other specieswhose genome information has already been released. One of thefuture challenges of genomics research will be to identify thepeculiarities of this species involved in environmental adaptationand toxigenic and pathogenic potential compared with the closelyrelated Fusarium spp. Many fundamental questions remain open.Has F. culmorum indeed lost its sexual cycle? What favours theshift in the F. culmorum/F. graminearum ratio in cereals? What isthe role of nonpathogenic populations of F. culmorum in confer-ring adaptation to their host plants and how do saprophyticstrains differ from pathogenic strains? Knowledge on the F. cul-morum chemotype distribution worldwide may help us to betterunderstand how chemotypes can be favoured by certain agrocli-matological conditions. Given the general lack of information onthe chemotype from the Southern Hemisphere and from world-wide populations of F. culmorum, it would be worth studying thechemotype distribution in relation to the host and to the diseasephases (i.e. FHB or FRR), and comparing this with isolates obtainedfrom undisturbed soils, in order to decipher the role of the chemo-type in the presence versus absence of agricultural selectionenvironments.

Finally, the identification of new natural and natural-like mol-ecules inhibiting trichothecene biosynthesis by F. culmorum,without affecting its vegetative growth, presents a vast array ofpractical applications. The bioavailability of inhibiting molecules



and the evidence that exposure in vitro to different concentrationsmay result in opposite effects (i.e. inhibition versus enhancementof trichothecene production; G. Delogu, unpublished data) mayprompt the development of new ecofriendly formulations toreduce the risk of these compounds being strongly affected byenvironmental conditions when applied in the field.

ACKNOWLEDGEMENTS

The authors acknowledge support by the Regione Autonoma della Sar-degna (Legge Regionale 7 agosto 2007, n. 7 ‘Promozione della ricercascientifica e dell’innovazione tecnologica in Sardegna’), the Ministry ofUniversity and Research (PRIN 2007 and 2011) and the Qatar NationalResearch Fund (a member of the Qatar Foundation; National PrioritiesResearch Program Grant # 4-259-2-083). MP acknowledges the AM2cprogram of the National Research Fund of Luxembourg. The authors wishto thank Renato D’Ovidio, Corby Kistler, Naresh Magan and anonymousreferees for critical review of the manuscript, and Kim Hammond Kosackand John Manners for sharing unpublished data on genome sequencinginitiatives. The statements made herein are solely the responsibility of theauthors.

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